Abstract
Diether and tetraether lipids are fundamental components of the archaeal cell membrane. Archaea adjust the degree of tetraether lipid cyclization in order to maintain functional membranes and cellular homeostasis when confronted with pH and/or thermal stress. Thus, the ability to adjust tetraether lipid composition likely represents a critical phenotypic trait that enabled archaeal diversification into environments characterized by extremes in pH and/or temperature. Here we assess the relationship between geochemical variation, core- and polar-isoprenoid glycerol dibiphytanyl glycerol tetraether (C-iGDGT and P-iGDGT, respectively) lipid composition, and archaeal 16S rRNA gene diversity and abundance in 27 geothermal springs in Yellowstone National Park, Wyoming. The composition and abundance of C-iGDGT and P-iGDGT lipids recovered from geothermal ecosystems were distinct from surrounding soils, indicating that they are synthesized endogenously. With the exception of GDGT-0 (no cyclopentyl rings), the abundances of individual C-iGDGT and P-iGDGT lipids were significantly correlated. The abundance of a number of individual tetraether lipids varied positively with the relative abundance of individual 16S rRNA gene sequences, most notably crenarchaeol in both the core and polar GDGT fraction and sequences closely affiliated with Candidatus Nitrosocaldus yellowstonii. This finding supports the proposal that crenarchaeol is a biomarker for nitrifying archaea. Variation in the degree of cyclization of C- and P-iGDGT lipids recovered from geothermal mats and sediments could best be explained by variation in spring pH, with lipids from acidic environments tending to have, on average, more internal cyclic rings than those from higher pH ecosystems. Likewise, variation in the phylogenetic composition of archaeal 16S rRNA genes could best be explained by spring pH. In turn, the phylogenetic similarity of archaeal 16S rRNA genes was significantly correlated with the similarity in the composition of C- and P-iGDGT lipids. Taken together, these data suggest that the ability to adjust the composition of GDGT lipid membranes played a central role in the diversification of archaea into or out of environments characterized by extremes of low pH and high temperature.
Highlights
Archaea inhabit environments characterized by extremes of salt, temperature, and pH
P-iGDGTs in hot spring sediments/mats with those obtained from surrounding soils, matrices describing the dissimilarity in the relative abundance of individual lipid structures (i.e., glycerol dibiphytanyl glycerol tetraethers (GDGTs)-0 to GDGT-8) were constructed and subjected to Mantel regression
Comparison of the compositions of C-iGDGT and P-iGDGTs obtained from both hot spring sediment/mat and surrounding soils revealed statistically insignificant relationships (Mantel R = 0.00 and 0.03, respectively; p-values = 0.79 and 0.98, respectively) (Figures 1C,D), indicating that the lipid structures identified in the hot spring sediment/mats are not likely to be the result of exogenous input
Summary
Archaea inhabit environments characterized by extremes of salt, temperature, and pH. The ecological dominance of archaea in these environments, including environments with characteristics (e.g., combined low pH and high temperature) that preclude bacterial colonization (Inskeep et al, 2010), has been suggested to result from the evolution of phenotypic traits that enable survival under conditions of chronic energy stress (Valentine, 2007). The lipid membrane is fundamental to energy generation and the maintenance of cellular homeostasis, suggesting that survival in these extreme environments requires highly specialized lipid membranes (van de Vossenberg et al, 1998; Macalady et al, 2004; Baker-Austin and Dopson, 2007). Archaea synthesize a variety of diether and tetraether linked membrane lipids (Yamauchi et al, 1993; Macalady et al, 2004; Valentine, 2007). The monolayer arrangement and the ether-linked bonding are thought to confer enhanced thermal stability to the lipid membrane (Thompson et al, 1992). Internal cyclopentyl rings are thought to enhance the thermal stability of the GDGT membrane through increased packing density (Gliozzi et al, 1983; Gabriel and Chong, 2000)
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